Table Of ContentR E S E A R C H A R T I C L E
Sensory Tricks in Primary Cervical Dystonia Depend on
Visuotactile Temporal Discrimination
Georg Ka€gi,MD,1,2 Petra Katschnig,MD,1,3 MirtaFiorio, PhD,4Michele Tinazzi,PhD,4,5
DianeRuge, MD,1 John Rothwell,PhD,1 Kailash P. Bhatia,MD1*
1SobellDepartmentofMotorNeuroscienceandMovementDisorders,InstituteofNeurology,QueenSquare,London,UnitedKingdom
2DepartmentofNeurology,KantonsspitalSt.Gallen,St.Gallen,Switzerland
3DepartmentofNeurology,MedicalUniversityofGraz,Graz,Austria
4DepartmentofNeurological,Neuropsychological,MorphologicalandMovementSciences,UniversityofVerona,Verona,Italy
5NeurologyUnit,BorgoTrentoHospital,Verona,Italy
1
ABSTRACT: A characteristic feature of primary ment to sensory tricks compared with the group with
cervical dystonia is the presence of ‘‘sensory tricks’’ partial improvement to sensory tricks. A significant
as well as the impairment of temporal and spatial sen- effect for group and modality and a significant interac-
sory discrimination on formal testing. The aim of the tion between group 3 modality were found, with lower
present study was to test whether the amount of visuotactile discrimination thresholds in the group with
improvement of abnormal head deviation due to a complete improvement to sensory tricks compared
sensory trick is associated with different performance with the other groups. In primary cervical dystonia, a
of temporal sensory discrimination in patients with cer- complete resolution of dystonia during a sensory trick
vical dystonia. We recruited 32 patients with cervical is associated with better visuotactile discrimination
dystonia. Dystonia severity was assessed using the To- and shorter disease duration compared with patients
ronto Western Spasmodic Torticollis Rating Scale. with less effective sensory tricks, which may reflect
Patients were rated according to clinical improvement progressive loss of adaptive mechanisms to basal gan-
to a sensory trick and assigned to 1 of the following glia dysfunction. VC 2013 Movement Disorder Society
groups: (1) no improvement (n 5 6), (2) partial
improvement (n 5 17), (3) complete improvement (n 5
9). Temporal discrimination thresholds were assessed Key Words: primary adult-onset cervical dystonia;
for visual, tactile, and visuotactile modalities. Disease temporal sensory discrimination; sensory trick; geste
duration was shorter (P 5.026) and dystonia severity antagoniste
lower (P 5.033) in the group with complete improve-
Dystonia is characterized by sustained involuntary (AOPCD) is the most common form of adult-onset
muscle contractions causing twisting and abnormal focal dystonia.2 The incidence is sex- and age depend-
posturing.1 Adult-onset primary cervical dystonia ent. Women are affected 1.5–1.9 times more often
than men, and in both men and women the peak inci-
dence is in the fifth decade. In addition to dysfunction
------------------------------------------------------------ of the basal ganglia, other brain regions such as the
*Correspondenceto:KailashP.Bhatia,ProfessorSobellDepartmentof cerebellum, thalamus, cerebral cortex, and midbrain/
MotorNeuroscienceandMovementDisorders,InstituteofNeurology,
brain stem may be involved in the etiology of dysto-
UniversityCollegeofLondon,QueenSquare,LondonWC1N3BG,UK;
[email protected] nia.3 A characteristic feature of primary dystonia and
Relevantconflictsofinterest/financialdisclosures:GeorgKa€giwas especially of adult-onset primary cervical dystonia is
supportedbyagrantfromtheSwissParkinson’sDiseaseAssociation
the improvement of dystonic contractions during a
andtheHalleyStewartTrust.
Fullfinancialdisclosuresandauthorrolesmaybefoundintheonline sensory maneuver (sensory trick), which can be
versionofthisarticle. observed in about three quarters of patients.4,5 In cer-
Received:4June2012;Revised:29October2012;Accepted: 5 vical dystonia, the sensory maneuver usually consists
November 2012 of touching the face contra- and/or ipsilateral to the
Publishedonline2January2013inWileyOnlineLibrary
(wileyonlinelibrary.com).DOI:10.1002/mds.25305 direction of head rotation, or sometimes even
356 MovementDisorders,Vol.28,No.3,2013
T E M P O R A L D I S C R I M I N A T I O N / S E N S O R Y T R I C K I N C D
imagination can reduce or abolish involuntary muscle Temporal discrimination thresholds were examined
activity.4,6,7 The presence of this phenomenon and with pairs of tactile, visual, and tactile/visual (cross-
that sensory abnormalities can be present led to the modal) stimuli. Square-wave electrical pulses, which
hypothesis that dystonia is not only a motor but also were delivered by a constant current stimulator (DS3,
a sensory disorder.8,9 In fact, patients with adult-onset Digitimer Ltd.) through surface skin electrodes (4 mm
primary focal dystonia have impaired spatial10 and in diameter) were used for tactile stimulation. The
temporal sensory discrimination,11 as indicated by electrodes were placed on the index and middle fingers
increased thresholds on standardized sensory testing. of both hands. The anode was 1.5 cm distal from the
Furthermore, there is good evidence from functional cathode. The intensity of tactile stimulation for each
imaging12 and from electrophysiological13 studies to subject and each finger was determined by delivering a
support this hypothesis. In the former study, dramatic series of stimuli with increasing intensity from 2 milli-
disorganization in the primary sensory cortex of non- amperes (mA) in steps of 1 mA. The minimal intensity
dystonic hand representation was found in all patients, at which electric stimuli were perceived in 10 of 10
and its amount paralleled the severity of dystonic limb stimuli was used in the experimental test. Care was
motor impairment.12 The latter study, investigating taken that stimuli did not induce pain or discomfort.
central sensory integration in dystonia using somato- Visual stimuli were delivered through light-emitting
sensory-evoked potentials, showed that the inhibitory diodes (LEDs) positioned on a black table. Subjects’
integration of afferent inputs, mainly proprioceptive, hands were positioned near the LEDs. Subjects were
coming from adjacent body parts is abnormal.13 asked to look at the fixation point in the middle
On the basis of the findings that a successful sensory between the LEDs throughout each trial. Both visual
trick requires sensory input to be processed and that and tactile stimuli lasted 5 ms. The experimental test
sensory discrimination can be impaired in primary was delivered in 6 combinations of stimulation: 2 tac-
dystonia, we hypothesized that the more the sensory tile (left and right), 2 visual (left and right), and 2
processing is impaired, the less successful the sensory crossmodal (visuotactile left and visuotactile right).
trick will be. The aim of this study was to test this hy- The order in which the 6 combinations of stimuli
pothesis on patients with adult-onset primary cervical were presented was randomized across the subjects.
dystonia, by measuring temporal sensory (visual, tac- Each combination of stimuli was performed in 4 sepa-
tile, visuotactile) discrimination. rate blocks. In the first trial of each block, pairs of si-
multaneous stimuli (interstimulus interval [ISI] ¼ 0
ms) were delivered. In subsequent trials, ISIs were pro-
gressively increased in steps of 10 ms. In each block
Patients and Methods
trials with simultaneous stimuli were interspersed to
check for attention.
We recruited patients with AOPCD who were
The temporal discrimination threshold was consid-
attending the movement disorder or botulinum toxin
ered the first of 3 consecutive ISIs during which sub-
clinics at the National Hospital for Neurology and
jects recognized the stimuli as asynchronous. In
Neurosurgery, London, as well as healthy controls.
addition, subjects were asked to judge which stimulus
After giving written consent, eligible patients were
preceded (or followed) the other. The first of 3 consec-
clinically examined by an experienced movement
utive ISIs during which subjects also reported correctly
disorders specialist (G.K.). Participants with clinical
the temporal order in a pair of stimuli was termed
evidence of polyneuropathy or carpal tunnel syndrome
temporal order judgment.
were excluded. Dystonia severity was quantified with
the Toronto Western Spasmodic Torticollis Rating
Statistical Analysis
Scale (TWSTRS), which is divided into 3 subscales.
Subscale I assesses motor severity, with a maximum Data were analyzed using SPSS Statistical Package
score of 35; subscale II assesses disability, with a max- for Windows version 14.0 and R statistical software
imum score of 30; and subscale III assesses pain sever- (version 2.9.0). Data are presented as mean and stand-
ity and its disability, with a maximum score of ard deviation of the mean for age, age at disease
20.14,15 To assess the effect of a sensory trick, the onset, disease duration, TWSTRS score, TWSTRS sub-
patients were asked to apply the most effective sensory scores I–III, visual-, tactile-, and crossmodal temporal
trick in their experience, which was rated as follows: discrimination thresholds, and temporal order judg-
0 points for an absent response, 1 point for some ments. One-way ANOVA with post hoc Bonferroni
effect, and 2 points for complete resolution of cervical test was applied with the sensory trick group as factor
dystonia during the sensory trick. The patients were and age, age of onset, disease duration, TWSTRS
assigned to 1 of the 3 groups according to the rating score, and subscores I–III as dependent variables.
of the sensory trick (no sensory trick, partial sensory Temporal discrimination thresholds (visual, tactile,
trick, or complete sensory trick). crossmodal) were first analyzed using a 3-way
MovementDisorders,Vol.28,No.3,2013 357
K A€G I E T A L .
TABLE1.Clinical and demographic data according to the sensory trick
Patients
NoST PartialST CompleteST NoSTvspartialSTP NoSTvscompleteSTP PartialSTvscompleteSTP
Number(%) 6(19) 17(53) 9(28) — — —
Female/male 4/2 13/4 7/2 1 1 1
Age 58.2610.1 55.769.7 56.8611.3 1 1 1
Ageofonset 42.568.5 40.8611.5 50.9610.9 1 .461 .094
Diseaseduration 15.7610.5 14.868.5 5.961.4 1 .067 .026
TWSTRStotal 23.6612.3 28.368.5 18.765.3 .767 .862 .033
TWSTRSsubscoreI 12.263.1 12.162.4 10.263.6 1 .639 .405
TWSTRSsubscoreII 6.764 8.963.9 6.664.7 .783 1 .530
TWSTRSsubscoreIII 6.365.8 7.464.3 1.962.2 1 .170 .009
Allvaluesaremeanswithstandarddeviationunlessstatedotherwise.
P<.05(ANOVAwithposthocBonferroni)inbold.
ANOVA model with time (in milliseconds) as the ms); tactile, 101.2 6 46.6 ms (women, 109.1 6 49.2
dependent variable and sensory trick group (no, par- ms; men, 77.6 6 28.5 ms); and crossmodal (visual/tac-
tial, complete sensory trick), modality (visual, tactile, tile), 141.3 6 39.3 ms (women, 142.7 6 33.2 ms;
crossmodal), and task (temporal discrimination thresh- men, 136.9 6 56.7 ms). No significant effect was
old, temporal order judgment) as explanatory varia- found for the factor sex for either of the evaluated
bles (fixed factors), including an interaction term variables. Six patients with adult-onset primary cervi-
between sensory trick group and modality. Post hoc cal dystonia (19%) were allocated to the no sensory
pairwise comparisons between the fixed factors were trick group, 17 patients (53%) to the partial sensory
performed using Tukey’s procedure. P < .05 was trick group, and 9 patients (28%) to the complete sen-
considered significant. In primary adult-onset primary sory trick group. As presented in Table 1, significant
cervical dystonia, existing literature suggests that sen- effects were found for the sensory trick group and dis-
sory discrimination thresholds depend on age but less ease duration (F ¼ 4.6, P ¼ .018), with a significantly
on disease severity or disease duration. Therefore, (P ¼ .026) shorter disease duration in patients with a
Pearson’s correlation coefficients were calculated to complete sensory trick compared with patients with a
characterize and test (without adjustment for multiple partial sensory trick in the post hoc analysis and for
testing) these associations. the TWSTRS score (F ¼ 3.8, P ¼ .035) and subscore
III (F ¼ 5.3, P ¼ .009) with significantly lower scores
in patients with a complete sensory trick compared
Results with patients with a partial sensory trick in the post
hoc analysis (P ¼ .033 and P ¼ .009, respectively).
Thirty-two patients (24 women, 8 men) with adult- No significant effects were found for age, age of onset,
onset primary cervical dystonia were included. The or TWSTRS subscores I and II.
mean age of patients was 56.4 6 9.9 years (women, The 3-way ANOVA model showed significant
56.3 6 9 years; men, 57 6 13.1 years), mean age of effects for the sensory trick group (F ¼ 6.2, P ¼ .002)
onset was 44 6 11.4 years (women, 44.4 6 9.6 years; and modality (F ¼ 101.8, P < .001) but not for task.
men, 42.5 6 16 years), and mean disease duration Therefore, temporal discrimination thresholds and
was 12.5 6 8.5 years (women, 11.8 6 8.5 years; men, temporal order judgments were averaged to further
14.5 68.9 years). Eighty-four percent of our study test the interaction sensory trick group (cid:2) modality,
population was right-handed. The mean TWSTRS which was significant (F ¼ 2.5, P ¼ .046). Post hoc
score was 24.7 6 9.3 (women, 25.9 6 9.6; men, 21.2 pairwise analysis of the interaction between sensory
6 8.2). An improvement in a sensory maneuver was trick group and modality showed significant differen-
present in 20 of 24 female patients (83%) versus 6 of ces in the crossmodal paradigm between the complete
8 male patients (75%). Mean temporal discrimination sensory trick and no sensory trick groups (P ¼ .049)
thresholds were: visual, 53.2 6 15.7 ms (women, 54.1 as well as between the complete sensory trick and par-
6 15.5 ms; men, 50.4 6 17.2 ms); tactile, 85.7 6 tial sensory trick groups (P ¼ .008), whereas no signif-
38.5 ms (women, 90.3 6 41.5 ms; men, 71.9 6 24.6 icant difference was found between the no sensory
ms); and crossmodal (visual/tactile), 134.5 6 38.7 ms trick and the partial sensory trick groups. Post hoc
(women, 135.4 6 32.1 ms; men, 131.8 6 56.7 ms). analysis did not show significant differences between
Mean temporal order judgments were: visual, 55.3 6 the sensory trick groups either for the visual or for the
16.2 ms (women, 56.5 6 16.4 ms; men, 51.7 6 16.2 tactile paradigms. Pairwise post hoc analysis between
358 MovementDisorders,Vol.28,No.3,2013
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TABLE 2.Electrophysiological results according to the sensory trick
Sensorytrick Visual(ms) Tactile(ms) Crossmodal(ms) Rowmean(ms)
Absent tdt 49.9613.4 97.2646.5 147.7624.4 98.3650.5
toj 53.9613.2 121.4652.5 152.9631.4 109.4654.4
Mean 51.9612.9 109.3648.9 150.3627.0 103.8618.2
Partial tdt 54.0615.2 89.7641.1 144.5642.8 96.0651.1
toj 54.8615.4 101.2646.5 150.6643.7 102.2654.2
Mean 54.4615.1 95.4643.6 147.5642.7 99.1616.2
Complete tdt 53.8619.3 70.5624.6 106.8623.9 77.0631.4
toj 57.2620.7 87.7643.2 115.9623.5 87.0638.4
Mean 55.5619.5 79.1635.3 111.4623.5 82.068.2
Allvaluesaremeanswithstandarddeviation.
ms,milliseconds;tdt,temporaldiscriminationthreshold;toj,temporalorderjudgment.
different modalities within the same sensory trick account for this discrepancy. Another important factor
group throughout showed significant differences, seems to be the differentiation between forcible (push-
except for the tactile versus the crossmodal paradigm ing against the direction of head deviation) and classic
in the group without sensory trick and the visual ver- (only light touch) sensory tricks. Ochudlo et al17 ana-
sus tactile paradigm in the complete sensory trick lyzed the relationship between clinical data in patients
group (Table 2). with forcible and classic sensory tricks separately. They
Among all patients, age correlated with visual tem- found that forcible sensory tricks were associated with
poral discrimination (temporal discrimination thresh- higher disease severity on the TWSTRS, whereas the
old: r ¼ 0.441, P ¼ .011; temporal order judgment: r opposite was true for patients with classic sensory
¼ 0.406, P ¼ .021) and with tactile temporal discrimi- tricks. The fact that we found less severe disease only
nation without reaching the level of significance (tem- in the complete sensory trick group compared with the
poral discrimination threshold: r ¼ 0.339, P ¼ 0.058; partial and no sensory trick groups seems to provide
temporal order judgment: r ¼ 0.343, P ¼ .054), but evidence that a sensory maneuver that releases dystonia
not with crossmodal temporal discrimination. Motor completely represents a classic sensory trick, whereas
disease severity, expressed by TWSTRS subscore I, partial sensory tricks seem to include more forcible sen-
and disease duration did not correlate with the tempo- sory tricks and therefore, from a pathophysiological
ral discrimination thresholds. point of view, are closer to the group without sensory
tricks than to the group with complete sensory tricks.
In the study by Martino et al,5 both forcible and classic
Discussion
sensory tricks were included.
One interesting result of the present study is that
Thispsychophysicalstudyonsensorytricksinpatients patients with a complete sensory trick performed
withadult-onsetprimarycervicaldystoniarevealedrele- significantly better in the crossmodal temporal discrimi-
vantfindingsthatrequirefurtherdiscussion. nation task, as expressed by lower thresholds, com-
In this study, patients with complete improvement to pared to patients with only a partial or absent effect to
a sensory maneuver had shorter disease duration and a a sensory trick. It is particularly interesting that only
lower TWSTRS score compared with patients with the crossmodal task revealed differences between the
only partially effective sensory tricks, whereas patients’ groups selected by the effect of a sensory maneuver,
age did not differ between the 3 groups (no, partial, whereas the unimodal tasks did not (see Fig. 1). This
complete sensory trick). The finding that patients with may relate to our finding that sensory tricks and sen-
a short disease duration experienced a better effect of a sory discrimination both deteriorate with increasing du-
sensory maneuver has been described in different types ration of disease. In contrast, when taken across the
of focal dystonia, such as cervical dystonia,6,16,17 writ- whole group of patients, unimodal temporal discrimi-
er’s cramp,18 and blepharospasm.19 The relationship of nation tasks were correlated with age (visual and a
disease severity and effectiveness of the sensory trick trend for tactile), but no correlation was found with
found in this study has also been found in other stud- disease severity and disease duration. In this context it
ies,6,17 whereas this relationship was not significant in should be noted that there is considerable variation in
another recent study on sensory tricks by Martino disease progression. Although loss of the sensory trick
et al.5 Because only the latter study applied the Burke- with longer disease duration is true for most patients
Fahn-Marsden score compared with the TWSTRS in with adult-onset primary cervical dystonia, there are
the other studies (our study included), differences in also patients who never lose or never experience the
the range of scores and in the validity might partly effect.
MovementDisorders,Vol.28,No.3,2013 359
K A€G I E T A L .
adult-onset primary cervical dystonia. They speculated
that the perceptual imbalance induced by the sensory
trick displaced the egocentric midvertical reference
toward the opposite side and increased ipsilateral pari-
etal activity.
These observations from functional imaging studies
showing that the parietal cortex, as an important
center of multimodal sensory integration, is hyperac-
tive during the execution of a sensory maneuver is
well in line with our findings of better performance
(lower temporal crossmodal [visual/tactile] discrimina-
tion thresholds) in patients with a complete sensory
trick compared to patients with less effective or absent
sensory tricks. This means that parietal function (mul-
timodal sensory integration) decreases with longer dis-
ease duration. As shown in the prepulse blink reflex
inhibition or in the fMRI experiments, the progressive
increase in temporal crossmodal discrimination thresh-
FIG. 1. Interaction plot with standard error of the estimates showing
the2-way interactions between modality and sensory trick after aver- olds may reflect progressive loss of cortical adaptive
agingtdtandtoj(absent,nosensorytrickgroup;partial,partial sen- mechanisms to the basal ganglia dysfunction of adult-
sorytrickgroup;complete,completesensorytrickgroup).
onset primary cervical dystonia. Our results provide
evidence that patient assignment according to their
sensory trick represents a different selection from a
pathophysiological point of view where the functional
The results of a number of other studies have consis-
integrity of the parietal cortex is important, which is
tently shown a relationship between processing of
reflected by the crossmodal sensory discrimination
sensory input and sensory tricks. One study investi-
thresholds.
gated patients with blepharospasm and found an asso-
In summary, this study confirms that in adult-onset
ciation between the presence of sensory tricks and
primary cervical dystonia, sensory tricks are more
normal prepulse inhibition of the blink reflex.20 In
prevalent in patients with short disease duration and
fact, in those experiments prepulse effects depended
less severe disease expressed by low TWSTRS score,
on activation of trigeminal afferents, consistent with
whereas it does not depend on the patient’s age. This
the idea that abnormal processing of that sensory
could be explained by intact sensory afferents in early
input is associated with the absence of the sensory
disease stages that get impaired the longer disease pro-
trick. Another fMRI study on patients with writer’s
gresses. On a cortical (parietal) level, functionally
cramp found increased activation of basal ganglia
intact adaptive mechanisms to the basal ganglia dys-
nuclei and various cortical areas (bilateral visual areas,
function seem to be a premise for the presence of a
contralateral anterior insula, and ipsilateral parietal
good clinical effect to a sensory maneuver, because
cortex [intraparietal sulcus]) during discrimination of
with its loss, crossmodal (visuo/tactile) temporal dis-
tactile stimuli. Interestingly, the effect was smaller in
crimination thresholds increase.
patients with a longer duration of symptoms but had
no correlation with clinical severity.18 One possible Acknowledgment: We thank Florent Baty from the Division of
explanation is that overactivation early in the course PulmonaryMedicine,KantonsspitalSt.Gallen,forhisstatisticaladvice.
of the disease represents recruitment of a compensa-
tory mechanism that declines in effectiveness over the References
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